Largo, Danilo B.

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SEAFDEC/AQD Institutional Repository (SAIR)This document is downloaded at: 2013-07-02 03:25:30 CSTTitle Recent developments in seaweed diseasesAuthor(s) Largo, Danilo B.CitationLargo, D.B. (2002). Recent developments in seaweed diseases. In: A.Q.Hurtado, N.G. Guanzon, Jr., T.R. de Castro-Mallare, & M.R.J. Luhan(Eds.) Proceedings of the National Seaweed Planning Workshop held onAugust 2-3, 2001, SEAFDEC Aquaculture Department, Tigbauan, Iloilo.(pp. 35-42). Tigbauan, Iloilo : SEAFDEC Aquaculture Department.Issue Date 2002URL http://hdl.handle.net/10862/196http://repository.seafdec.org.phRecent Developments in Seaweed DiseasesDanilo B. LargoDepartment of BiologyUniversity of San Carlos, Talamban, Cebu City, PhilippinesEmail: biology@mangga.usc.edu.phMost of what we know about seaweed diseases is generally focused on those affecting theEucheuma/Kappaphycus seaweed, particularly the "ice-ice" disease phenomenon. However, muchof our knowledge about seaweed diseases are mainly those observed in non-eucheumatoid algae,especially those cultivated for use as food in Japan, China and Korea namely Porphyra, Gracilaria, and Laminaria. These diseases vary in terms of their causative agents and manifestations. Table 1 shows the different species of cultivated seaweeds around the world that are known to be affectedby microbial pathogens after being pre-disposed by certain factors.* for details regarding the author, contact Dr. Danilo Largo at the above address. Table 1. Diseases in commercial seaweeds caused by bacteria and other microorganismsHost seaweedPorphyra tenera Porphyra sp.P. yezoensis Laminaria sp.Gracilaria sp.G. conferta G. chilensis Chondrus crispus Kappaphycus/EucheumaName of diseasewhite rot disease"suminori"disease"anaaki" or "pin-hole disease"malformationdisease"rotten thallussyndrome""white rot""white tips disease"lesion/bleaching"green rot" or"green spot disease""ice-ice"Suspectedcausative agentBeneckia(=Vibrio)Flavobacterium sp.Flavobacterium sp.unidentifiedbacteriaVibrio sp.amoeba-likeorganismunidentifiedbacteriumagarolytic bacterialstraindeep orangecolored bacteriaVibrio sp. P11,Cytophaga sp. P25Environmentalcondition priorto outbreakexposure to lowtemperature atextended low tideperiodhigh temperaturelow summertemperaturehigh H2S contentreduced flow ratein culture tankexposure to hightemperature andhigh lightintensitysurface wounds bymechanical orbiological activitieslow salinity, lowlight intensityAuthor*Tsukidate 1983Kusuda et al.1992Sunairi et al.1995Uchida & Nakayama 1993Lavilla-Pitogo1992Correa & Flores1995Weinberger etal. 1994Craigie 1995Craigie & Correa1996Largo et al.1995a, 1995bProceedings of the National Seaweed Planning Workshop Andrews (1976) defined seaweed disease as "a continuing disturbance to the plant's normalstructure and function such that it is altered in growth rate, appearance, or economic importance".Is this definition good enough to include the "ice-ice" disease in Eucheuma/Kappaphycus? "Ice-ice", as some of us are familiar with, affects not only growth but also its appearance and, possibly,carrageenan product quality. Perhaps, your definition of "ice-ice" disease is as good as this definitionby Andrews.There are two kinds of diseases in plants: infectious and non-infectious type. The formerinvolves a transmissible infectious agent (bacteria, fungi, virus, etc.) while the latter is induced byphysiogenic factors such as extremes of temperature, salinity, light intensity or pollution. Otherthan those in economic seaweeds, most of what is known to be diseases in macroalgae are thetypes that are generally less threatening to the natural seaweed population. In 1992, however, a form of an algal disease, known as coralline lethal orange disease (or CLOD), caused by anunidentified motile bacterium, consumed a large population of reef-building coralline algae in theSouth Pacific (Littler and Littler 1994, 1995). This phenomenon underscores the potential of a bacterial pathogen not only to the coral reef ecology but also to the cultivated seaweed species.Local seaweed species face the similar threat of an infectious type of a disease considering thetraditional method of propagating Eucheuma/Kappaphycus, since seaweed cultivation started inthe Philippines in the late 1960's. The genetic implication of clonal propagation in these seaweedslies in the tendency of some species to become susceptible to a potential pathogen (Santelices1992). An "early warning device" in seaweed farming against potential pathogens, such as bacteria,is therefore crucial in the management of seaweed farms. Any approach to this problem would lieon the understanding of the whole seaweed pathosystem in the context of host-pathogen interaction.There are two important disorders seen in Eucheuma/Kappaphycus cultivation that haveespecially caused problems in recent year. These are:"Ice-ice" disease. "Ice-ice" is generally caused by unfavorable environmental conditions inthe planting site. This is a rather general statement because "unfavorable factors" in the cultivationsite refers either to high or low temperature, high or low salinity, high or low light intensity, andalso to insufficient nutrient, and so forth. Addressing any of these factors is considered a managementintervention strategy. So far, the role of temperature, salinity and light intensity, taken singly wasobserved in controlled laboratory set up as possible predisposing factors that can lead to "ice-ice"disease. The role of microbial pathogens has also been shown as having to do with "ice-ice". In myown study of the role of bacteria as a lead factor in "ice-ice" disease development, it was discoveredthat normal (resident) bacteria could become opportunistic pathogens under certain conditions.Subliminal environmental factors (e.g. low salinity, or low light intensity) although in itself maynot readily lead to the disease manifestation could predispose the seaweed to bacterial attack,mainly by certain opportunistic pathogens. The seaweed-bacterial pathogen interaction could beakin to those in terrestrial plants. Could it be possible that a highly virulent pathogen is responsiblefor the wholesale destruction of cultivated seaweed crops in the Philippines? Normally, the surfacesof submerged plants are areas readily colonized by bacteria but only a few strains could be potentialpathogens. In the case of Eucheuma, two such bacterial pathogens belonging to the Vibrio-Aeromonas complex and the Cytophaga-Flavobacterium complex demonstrate the seaweed-bacteria interaction (Largo et al. 1995b). Strains of these two groups of bacteria can induce theice-ice disease in Eucheuma when the seaweed plant is subjected to stressful factor of either low36Recent Developments in Seaweed Diseasessalinity or low light intensity in suboptimal level. While Cytophaga sp. P25 showed non-motilebehavior, cells of Vibrio sp. P11 are active swimmers. This motile behavior of Vibrio makes suchbacterium an efficient seaweed surface invader. We theorized that it produces hydrolytic enzymeagainst carrageenan - the compound that makes up the bulk of the cells' interstitial matrices. IndeedVibrio sp. P11 when cultured in a medium of carrageenan instead of agar grows quite well. Thisability to digest carrageenan enables the bacterium to penetrate the inner region of the seaweedthallus. I believe that by its lytic activity, it starts digesting epidermal cells, destroying plastidsbearing the pigments, hence, the initial bleaching manifestation of the infected part. This leads togradual hydrolyses of the thallus starting from the cortical layer and into the medulla leading tonecrosis (tissue death). There could be other bacteria with similar ability as Vibrio sp. P l l thatneeds to be isolated.In recent years, many seaweed farms ceased to exist because of the "ice-ice" problem. Thishas been happening in Bohol, in Batangas, and even in Iloilo. Was it not that widespread "ice-ice"events, if you remember well, took place during the El Niño and La Niña seasons? What is theprobability of "ice-ice" not being caused by microbial pathogens?.Epiphyte infestation. Epiphytes refer to organisms, small or large, that colonize the surfacesof seaweeds. A serious case of epiphytism has been reported very recently in Calaguas Is., CamarinesNorte, and in many parts of the Bicol region. Is this another threat to seaweed farming? Figure 1 shows a common red algal epiphyte, Polysiphonia (with dark arrows) and diatoms (broken-linearrow) on Kappaphycus thalli. The Polysiphonia epiphytes create small, slightly elevated poreson the surface. These pores give "goosebumps" appearance on the thalli surface.Figure 1. A red algal epiphytes (left away) Polysiphonia and diatoms (right away) on Kappaphycus thalli.37Proceedings of the National Seaweed Planning Workshop Microscopic examination of a sectioned thallus (Figure 2) shows that these pores are actuallysites of penetration of the epiphytes (with arrows). Whether or not this filamentous alga takes on a more elaborate habit as an endophytic plant will be a subject for future investigation.Figure 2. Microscopic examination of sectioned thallus showing actual sites of penetration of the epiphytes,(shown with arrows)Primary considerations in the diagnosis of disease in seaweedsAndrews and Goff (1984) recommend that diagnosis, in order to determine symptomatologyof a seaweed disease, should not be attempted without familiarity with the algal host affected,preferably by personal experience or, as a minimum, by the study of publications on the growth ofthe plant and the biotic factors affecting its development. The following needs to be considered:• the direct or indirect role of environmental factors in disease development;that cases in which a primary pathogen is involved such that the disease can be relativelyeasily diagnosed by symptom (expressions of the host) or signs (visible evidence of thepathogen) will likely be rare;• that several different diseases may occur concurrently; and• that visual diagnosis is limited because similar symptoms may result from different agentsand, conversely, the same agent (particularly if abiotic) may induce different symptomsin different algae.38Recent Developments in Seaweed DiseasesIt is also important that the suspected organism first satisfies the Koch's postulate to determinewhether or not the organism is really a pathogen or not. The following steps are needed to addressthe Koch's postulate:• The causal agent must be associated in every case with the disease under natural conditionsand, conversely, the disease must not appear in the absence of the agent• The causal agent must be isolated in pure culture and characterized• Typical symptoms must develop when the host is inoculated with the agent under suitableconditions, and the appropriate control inoculations be concurrently made• The causal agent must be re-isolated and demonstrated to be identical to the agent isolatedoriginallyIn the case of "ice-ice", the disease may not be necessarily caused by a specific bacterialpathogen. In fact several bacteria, as was shown for Vibrio sp. PH and Cytophaga sp. P25 canplay a trigger role.Detection of pathogenic organismsThe detection system of a pathogen still relies on the culturability of the organism in an agarmedium. Unfortunately, this does not assure the unequivocal proof of association of the suspectedpathogen with the host. Biomolecular probe as used in the medical field in detecting diseaseorganisms is yet to be established in seaweed pathology. The potential use of immunology-basedtechniques has been attempted in seaweeds to detect and monitor the pathogen in the host plant.Direct detection of bacteria, i.e. without agar culture, for instance, has been used to monitor theVibrio sp. P11 in Kappaphycus alvarezii (Largo et al. 1998) and in Gracilaria species. The methodof detection, which utilizes polyclonal antibodies (rendered visible with the use of fluorescent dyesuch as FITC), was found to be quite effective in establishing the growth behavior of the organismin the thallus. This technique could be made as a practical tool to monitor suspected pathogens.However, it is necessary that the antibodies developed against the target organism should be highlyspecific and does cross-react with other organisms, either closely or distantly related."Ice-ice" disease triggered by bacteria could take place under the following conditions:• If there is slow water movement in the cultivation ground. Some pathogens, especiallybacteria, are highly motile and can very easily invade seaweed surfaces. Strong watercurrent, aside from enhancing nutrient exchange, also prevents potential pathogen thatcomes from the surrounding water from establishing on the seaweed surface (Largo et al.1997).• If the cultivation ground is close to freshwater sources, such as rivers or creeks. Thispractically reduces the salinity of the seawater below normal and a stressful factor to theseaweed (Largo et al. 1995a). These places are not the desirable sites for Eucheuma farming since it has a normal water salinity requirement of between 33-35 ppt.39Proceedings of the National Seaweed Planning Workshop • If water temperature is high, especially if this is accompanied by high light intensity. This is also stressful to the seaweed. This can be remedied by moving the plants to a slightly deeper location, but not too deep to dampen growth performance. Normaltemperature requirement for Eucheuma is between 25-31°C.Although each of the above factors could act independently from each other, they could actsynergistically, intensifying the development of "ice-ice" (Largo et al. 1995a). • Possible management interventionCrop management will tell us that to optimize production, any crop has to be grown at theplant's optimal growth requirement, with optional external investments on energy. Any factor thattends to deviate from this simple rule will produce bad crop that is below sustainable level.Some suggestions to properly manage the Eucheuma crop:• Avoid overcrowding plants in cultivation. This renders them susceptible to opportunisticpathogens, like some Vibrios and Cytophagas. Less crowding of plants also enhanceslight penetration and therefore to growth.• Stay within the optimal growth requirements of Eucheuma. Drastic changes in salinityand water temperature have to be avoided.• In times of very high light intensity, as during summer period, especially during El Niño seasons it may be advisable to move plants to a deeper location where light intensity doesnot lead to photoinhibition. Ways to improve planting techniques in such a way thatEucheuma crop can be easily moved need to be studied. El Niño season is destructive toseaweed cultivation, hence measures to prevent "ice-ice" need to be in place.• There is a need to identify more "ice-ice" disease-resistant strains of Eucheuma. The"sakol" variety of Kappaphycus alvarezii seems to have this property. New Eucheuma strains from protoplast fusion out of disease-resistant variety are expected to have thisdesirable characteristic.Future direction in the study of seaweed diseasesIt is clear that seaweed diseases could have a possible effect on seaweed cultivation in thePhilippines. Based on our current knowledge of seaweed pathosystem, it is realized that muchremains to be pursued in addressing the problems associated with seaweed farming. The followingare suggested:• Research on seaweed diseases and other disorders should be intensified in order to addressspecific problems related to health management• The reported phenomenon of intense epiphyte infestation in Eucheuma farming (e.g. inCalaguas Island, Camarines Norte) is an emerging problem that needs closer monitoring40Recent Developments in Seaweed Diseases• More screenings of potential pathogens based on Koch's postulate should be conducted• Innovative techniques in the detection of potential pathogens of "ice-ice" should enhancethe capability of farmers to monitor possible outbreaks of diseases• Management strategies in seaweed farming should anchor on sound scientific basesReferencesAndrews, JH. 1976. The pathology of marine algae. Biol. Rev. 51: 211-253Andrews, JH and LJ Goff. 1984. Pathology. In: M.M. Littler and D.S. Littler (Eds), Handbook of PhycologicalMethods. Ecological Field Methods: Macroalgae. Cambridge University Press, pp. 573-591Correa, JA and V Flores. 1995. Whitening, thallus decay and fragmentation in Gracilaria chilensis associatedwith an endophytic amoeba. J. Appl. Phycol. 7:421-425Craigie, JS and JA Correa. 1996. Etiology of infectious diseases in cultivated Chondrus crispus (Gigartinales,Rhodophyta) Hydrobiologia 326/327: 97-104Jeffray, AE and VE Coyne. 1996. Development of an in situ assay to detect bacterial pathogens of the redalga Gracilaria gracilis (Stackhouse). Steentoft. Irvine et Farnham. J. Appl. Phycol. 8: 409-414Kusuda, R, K Kawai, F Salati, Y Kawamura, and Y Yamashita. 1992. Characteristics of Flavobacterium sp.causing "suminori" disease in cultivated Porphyra. Suisanzoshoku 40: 457-461Largo, DB, K Fukami, T Nishijima and M Ohno. 1995a. Laboratory-induced development of the "ice-ice"disease of the farmed red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae,Gigartinales, Rhodophyta). J. Appl. Phycol. 7: 539-543Largo, DB, K Fukami, and T Nishijima. 1995b. Occasional pathogenic bacteria promoting "ice-ice" diseasein the carrageenan-producing red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae.Gigartinales, Rhodophyta). J. Appl. Phycol. 7: 545-554Largo, DB, K. Fukami, M Adachi and T Nishijima. 1997. Direct enumeration of total bacteria from macroalgaeby epifluorescence microscopy as applied to the fleshy red algae Kappaphycus alvarezii (Doty) andGracilaria spp. (Rhodophyta). J. Phycol. 33: 554-557Largo, DB, K Fukami, M Adachi and T Nishijima. 1998. Immunofluorescent detection of "ice-ice" disease-promoting bacterial strain Vibrio sp. P11 of the farmed macroalga, Kappaphycus alvarezii (Gigartinales.Rhodophyta). J. Mar. Biotechnol. 6: 178-182Lavilla-Pitogo, CR. 1992. Agar-digesting bacteria associated with 'rotten thallus syndrome' of Gracilaria sp. Aquaculture 102: 1-7Littler, MM and DS Littler. 1994. A pathogen of reef-building corraline algae discovered in the SouthPacific. Coral Reefs 13: 202Littler, MM and DS Littler. 1995. Impact of a CLOD pathogen on Pacific coral reefs. Science 267: 1356-136041Proceedings of the National Seaweed Planning Workshop Santelices, B. 1992. Strain selection of clonal seaweeds. In: F.E. Round and D.J. Chapman (Eds), Progressin Phycological Research 8: 85-116Sunairi, M, H Tuchiya, Y Omura, M Ozawa, N, Iwabuchi, H Murooka and M Nakajima. 1995. Isolation ofa bacterium that causes anaaki disease of the red algae Porphyra yezoensis. J. Appl. Bact. 79: 225-229Tsukidate, J. 1983. On the systematic relationship between Porphyra species and attached bacteria andbacterial pathogen in white rot. Bull. Nansei Reg. Fish. Res. Lab. 15: 29-96Uchida, M and A Nakayama. 1993. Isolation of Laminaria-frond decomposing bacteria from Japanese CoastalWaters. Nippon Suisan Gakkaishi 59: 1865-1871Weinberger, F, M Freidlander, and W Gunkel. 1994. A bacterial facultative parasite of Gracilaria conferta. Dis. Aquat. Org. 18: 135-14142

Agar-digesting bacteria associated with 'rotten thallus syndrome' of Gracilaria sp.

causing &quot;suminori&quot; disease in cultivated Porphyra.

Direct enumeration of total bacteria from macroalgae by epifluorescence microscopy as applied to the fleshy red algae Kappaphycus alvarezii (Doty) and Gracilaria spp.

Recent developments in seaweed diseases

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